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Miller was brought up in the St John's Wood area of North London and left school at the age of 16 to work in an estate agency. Shortly thereafter, he was spotted as a business talent by George Farrow who ran a small property company called Peachey. Farrow recruited Miller to work for him, and after Farrow's retirement, Miller became Chairman of Peachey.

Under Miller's guidance, Peachey Property Corporation took over many other companies and became the predominant freeholder for high-end leasehold properties in London. In the early 1960s, a sudden change in policy led Peachey to sell off some of the residential property in an attempt to become a major player in the commercial property field (then undergoing a boom). This attempt was not particularly successful. Miller was the developer of the Churchill Hotel in Portman Square for the Loews US Corporation.

Miller's father had been a Labour Party councillor and he also supported the party. In the early 1970s, Eric Miller began contributing to the running of Harold Wilson's private office and became a close personal supporter. He was appointed to the board of Labour Party Properties and served as Treasurer of the Socialist International. He was also a long serving director of Fulham F.C.

He received a knighthood in Wilson's retirement Honours list in 1976 (the controversial 'Lavender List'). However, rumours were already growing that the financial dealings of his companies had not been above board, and his inclusion in the list was criticised. Investigations uncovered the siphoning off of large sums from the Peachey Property Corporation, and Miller was forced from the chairmanship and eventually off the Peachey board entirely in early 1977. The Fraud squad and Department of Trade launched investigations, and Miller was served with four writs seeking restitution of funds he had allegedly taken. Miller committed suicide, by shooting himself on the Jewish Day of Atonement.